Preen gland secretions spread on the feathers contain various chemical compounds dominated by fatty acids (FAs) and volatile organic compounds (VOCs). These chemicals may significantly affect plumage condition, microbial and ectoparasitic load on feathers, and chemical communication of birds. However, how chemical composition of preen secretions varies in commercially produced chickens with respect to their genotype, sex, and feeding regime remain largely unknown, as well as the welfare implications for farmed poultry. We found that while polyunsaturated fatty acids in chicken preen secretions differed significantly with genotype (P << 0.001), saturated fatty acids and monounsaturated fatty acids varied with genotype-dependent preen gland volume (P < 0.01). Chickens of meat-type fast-growing Ross 308 genotype had reduced preen gland volume and lower proportions of all FA categories in their preen secretions compared with dual-purpose slow-growing ISA Dual chickens. A total of 34 FAs and 77 VOCs with tens of unique FAs were detected in preen secretions of both genotypes. While differences in the relative proportion of 6 of the 10 most dominant VOCs in chicken preen gland secretions were related to genotype (P < 0.001), only 1 of the 10 most dominant VOCs showed a sex effect (P < 0.01), and only 2 of the 10 most dominant VOCs showed a genotype-dependent effect of feed restriction (P < 0.05). Feed restriction had no effect on the relative proportion of any of the FAs in chicken preen gland secretions. Moreover, we found that meat-type Ross 308 preen secretions were dominated by VOCs, which are proven attractants for poultry red mite and may also increase infestation with other ectoparasites and negatively influence overall odor-mediated intraspecific communication and welfare. This study shows that no feeding management, but long-term genetic selection in commercial breeding may be the main cause of the differences in the biochemistry and function of chicken preen secretions. This might have negative consequences for chemosignaling, antiparasitic, and antimicrobial potential of preen secretions and can lead to increased susceptibility to ectoparasites, plumage care disorders, and can affect the overall condition, welfare, and productivity of commercially bred chickens. Selection-induced preen gland impairments must therefore be considered and compensated by proper management of the chicken farm and increased care about animal well-being.

The preen gland is the largest sebaceous gland in birds, which produces a secretion that is spread on the feathers during comfort behavior. The secretion of the preen gland contains various chemical compounds that are responsible for mechanical, antimicrobial, and antiparasitic protection of the plumage and probably also for chemical communication between birds. However, there are only a limited number of studies on the composition and function of preen secretions in wild birds and only limited evidence in poultry. In this study, we compared the chemical composition of preen secretions in fast-growing meat-type and slow-growing dual-purpose chickens and evaluated the effect of sex, body condition, and feeding regime on preen secretion composition. Fast-growing meat-type chickens had smaller preen glands and lower proportions of all analyzed compounds in preen secretions compared to slow-growing dual-purpose chickens. In addition, compounds that are proven attractants for a poultry-threatening ectoparasite, poultry red mite, were predominant in the secretions of meat-type chickens. This study is the first to show that genetically distinct breeds of chickens can differ significantly in the biochemistry of preen secretions, which can influence susceptibility to ectoparasites, plumage care disorders, and can affect the overall condition, well-being, and productivity of commercially raised chickens.

Department of Agroenvironmental Chemistry and Plant Nutrition Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague 6 Suchdol Czech Republic

Department of Animal Science Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague 6 Suchdol Czech Republic

Department of Food Science Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague 6 Suchdol Czech Republic

Department of Zoology and Fisheries Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague 6 Suchdol Czech Republic

Groningen Institute for Evolutionary Life Sciences University of Groningen 9747 AG Groningen The Netherlands

Institute of Vertebrate Biology of the Czech Academy of Sciences 603 65 Brno Czech Republic

See more in PubMed

Ajuyah, A. O., Lee K. H., Hardin R. T., and Sim J. S.. . 1991. Changes in the yield and in the fatty-acid composition of whole carcass and selected meat portions of broiler-chickens fed full-fat oil seeds. Poult. Sci. 70:2304–2314. doi:10.3382/ps.0702304 DOI

Alt, G., Mägi M., Lodjak J., and Mänd R.. . 2020. Experimental study of the effect of preen oil against feather bacteria in passerine birds. Oecologia 192:723–733. doi:10.1007/s00442-020-04599-8 PubMed DOI

Amo, L., Avilés J. M., Parejo D., Peña A., Rodríguez J., and Tomás G.. . 2012. Sex recognition by odour and variation in the uropygial gland secretion in starlings. J. Anim. Ecol. 81:605–613. doi:10.1111/j.1365-2656.2011.01940.x PubMed DOI

Apandi, M., and Edwards H. M.. . 1964. Studies on composition of secretions of uropygial gland of some avian species. Poult. Sci. 43:1445–1462. doi:10.3382/ps.0431445 DOI

Asproni, P., Bienboire-Frosini C., Barthelemy H., Mechin V., Teruel E., Leclercq J., Cozzi A., and Pageat P.. . 2020. Single fluff-spray application of mother hen uropygial secretion analogue positively influences bursa of Fabricius development. Poult. Sci. 99:6300–6306. doi:10.1016/j.psj.2020.08.076 PubMed DOI PMC

Bandyopadhyay, A., and Bhattacharyya S. P.. . 1996. Influence of fowl uropygial gland and its secretory lipid components on growth of skin surface bacteria of fowl. Indian J. Exp. Biol. 34:48–52. PubMed

Bandyopadhyay, A., and Bhattacharyya S. P.. . 1999. Influence of fowl uropygial gland and its secretory lipid components on the growth of skin surface fungi of fowl. Indian J. Exp. Biol. 37:1218–1222. PubMed

Bates, D., Mächler M., Bolker B., and Walker S.. . 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw 67:1–48. doi:10.18637/jss.v067.i01 DOI

Ben-Gigi, R., Haron A., Shinder D., Ruzal M., and Druyan S.. . 2021. Differential physiological response of slow- and fast-growing broiler lines to hypoxic conditions during chorioallantoic membrane development. Poult. Sci. 100:1192–1204. doi:10.1016/j.psj.2020.10.068 PubMed DOI PMC

Bernier, U. R., Allan S. A., Quinn B. P., Kline D. L., Barnard D. R., and Clark G. G.. . 2008. Volatile compounds from the integument of White Leghorn Chickens (Gallus gallus domesticus L.): candidate attractants of ornithophilic mosquito species. J. Sep. Sci. 31:1092–1099. doi:10.1002/jssc.200700434 PubMed DOI

Birkett, M., Pickett J., Dewhirst S., Jespersen J. B., and Kilpinen O. Ø.. . 2010. Use of a carboxylic acid or an aldehyde. World Intellectual Property Organization.

Bodawatta, K. H., Schierbech S. K., Petersen N. R., Sam K., Bos N., Jønsson K. A., and Poulsen M.. . 2020. Great tit (Parus major) uropygial gland microbiomes and their potential defensive roles. Front. Microbiol. 11:1735. doi:10.3389/fmicb.2020.01735 PubMed DOI PMC

Bokkers, E. A. M., and Koene P.. . 2003. Behaviour of fast- and slow growing broilers to 12 weeks of age and the physical consequences. Appl. Anim. Behav. Sci. 81:59–72. doi:10.1016/S0168-1591(02)00251-4 DOI

Bonadonna, F., Miguel E., Grosbois V., Jouventin P., and Bessiere J. M.. . 2007. Individual odor recognition in birds: an endogenous olfactory signature on petrels’ feathers? J. Chem. Ecol. 33:1819–1829. doi:10.1007/s10886-007-9345-7 PubMed DOI

Bonadonna, F., and Sanz-Aguilar A.. . 2012. Kin recognition and inbreeding avoidance in wild birds: the first evidence for individual kin-related odour recognition. Anim. Behav. 84:509–513. doi:10.1016/j.anbehav.2012.06.014 DOI

Braun, M. S., Sporer F., Zimmermann S., and Wink M.. . 2018. Birds, feather-degrading bacteria and preen glands: the antimicrobial activity of preen gland secretions from turkeys (Meleagris gallopavo) is amplified by keratinase. FEMS Microbiol. Ecol. 94:1–14. doi:10.1093/femsec/fiy117 PubMed DOI

Campagna, S., Mardon J., Celerier A., and Bonadonna F.. . 2012. Potential semiochemical molecules from birds: a practical and comprehensive compilation of the last 20 years studies. Chem. Senses 37:3–25. doi:10.1093/chemse/bjr067 PubMed DOI

Chauve, C. 1998. The poultry red mite Dermanyssus gallinae (De Geer, 1778): current situation and future prospects for control. Vet. Parasitol. 79:239–245. doi:10.1016/s0304-4017(98)00167-8 PubMed DOI

Czirják, G. A., Pap P. L., Vágási C. I., Giraudeau M., Mureşan C., Mirleau P., and Heeb P.. . 2013. Preen gland removal increases plumage bacterial load but not that of feather-degrading bacteria. Naturwissenschaften 100:145–151. doi:10.1007/s00114-012-1005-2 PubMed DOI

Delius, J. D. 1988. Preening and associated comfort behavior in birds. Ann. N. Y. Acad. Sci. 525:40–55. doi:10.1111/j.1749-6632.1988.tb38594.x PubMed DOI

Douglas, H. D.3rd, Co J. E., Jones T. H., and Conner W. E.. . 2001. Heteropteran chemical repellents identified in the citrus odor of a seabird (crested auklet: Aethia cristatella): evolutionary convergence in chemical ecology. Naturwissenschaften 88:330–332. doi:10.1007/s001140100236 PubMed DOI

Douglas, H. D.3rd, Co J. E., Jones T. H., and Conner W. E.. . 2004. Interspecific differences in Aethia spp. auklet odorants and evidence for chemical defense against ectoparasites. J. Chem. Ecol. 30:1921–1935. doi:10.1023/b:joec.0000045586.59468.de PubMed DOI

Douglas, H. D.3rd, Co J. E., Jones T. H., Conner W. E., and Day J. F.. . 2005. Chemical odorant of colonial seabird repels mosquitoes. J. Med. Entomol. 42:647–651. doi:10.1093/jmedent/42.4.647 PubMed DOI

Fischer, I., Haliński P., Meissner W., Stepnowski P., and Knitter M.. . 2017. Seasonal changes in the preen wax composition of the Herring gull Larus argentatus. Chemoecology 27:127–139. doi:10.1007/s00049-017-0239-z PubMed DOI PMC

Fulop, A., Czirjak G. A., Pap P. L., and Vagasi C. I.. . 2016. Feather-degrading bacteria, uropygial gland size and feather quality in House Sparrows Passer domesticus. Ibis 158:362–370. doi:10.1111/ibi.12342 DOI

Gabirot, M., Buatois B., Muller C. T., and Bonadonna F.. . 2018. Odour of king penguin feathers analysed using direct thermal desorption discriminates between individuals but not sexes. Ibis 160:379–389. doi:10.1111/ibi.12544 DOI

Gabirot, M., Raux L., Dell’Ariccia G., Bried J., Ramos R., J. ­Gonzalez-Solis, Buatois B., Crochet P. A., and Bonadonna F.. . 2016. Chemical ­labels differ between two closely related hearwater taxa. J. Avian Biol. 47:540–551. doi:10.1111/jav.00853 DOI

Gay, M., Lempereur L., Francis F., and Caparros Megido R.. . 2020. Control of Dermanyssus gallinae (De Geer 1778) and other mites with volatile organic compounds, a review. Parasitology 147:731–739. doi:10.1017/S0031182020000530 PubMed DOI PMC

Gebauer, A., Jacob J., Kaiser M., and Eck S.. . 2004. Chemistry of the uropygial gland secretion of Hume’s Ground Jay Pseudopodoces humilis and its taxonomic implications. J. Ornithol. 145:352–355. doi:10.1007/s10336-004-0030-0 DOI

Giraudeau, M., Czirják G., Duval C., Bretagnolle V., Gutierrez C., Guillon N., and Heeb P.. . 2013. Effect of preen oil on plumage bacteria: an experimental test with the mallard. Behav. Processes 92:1–5. doi:10.1016/j.beproc.2012.08.001 PubMed DOI

Giraudeau, M., Stikeleather R., McKenna J., Hutton P., and McGraw K. J.. . 2017. Plumage micro-organisms and preen gland size in an urbanizing context. Sci. Total Environ. 580:425–429. doi:10.1016/j.scitotenv.2016.09.224 PubMed DOI

Goldstein, D. L. 1988. Estimates of daily energy-expenditure in birds - the time-energy budget as an integrator of laboratory and field studies. Am. Zool. 28:829–844. doi:10.1093/icb/28.3.829 DOI

Goluke, S., and Caspers B. A.. . 2017. Sex-specific differences in preen gland size of zebra finches during the course of breeding. Auk 134:821–831. doi:10.1642/AUK-17-12.1 DOI

Haribal, M., Dhondt A., and Rodriguez E.. . 2009. Diversity in chemical compositions of preen gland secretions of tropical birds. Biochem. Syst. Ecol. 37:80–90. doi:10.1016/j.bse.2008.12.005 DOI

Hirao, A., Aoyama M., and Sugita S.. . 2009. The role of uropygial gland on sexual behavior in domestic chicken Gallus gallus domesticus. Behav. Processes 80:115–120. doi:10.1016/j.beproc.2008.10.006 PubMed DOI

Hwang, Y. S., Schultz G. W., Axelrod H., Kramer W. L., and Mulla M. S.. . 1982. Ovipositional repellency of fatty-acids and their derivatives against Culex Diptera, Culicidae and Aedes Diptera, ­Culicidae mosquitos. Environ. Entomol. 11:223–226. doi:10.1093/ee/11.1.223 DOI

Jacob, J. 1975. TLC, GLC and MS of complex lipid mixtures from uropygial secretions. J. Chromatogr. Sci. 13:415–422. doi:10.1093/chromsci/13.9.415 PubMed DOI

Jacob, J., Balthazart J., and Schoffeniels E.. . 1979. Sex-differences in the chemical composition of uropygial gland waxes in domestic ducks. Biochem. Syst. Ecol. 7:149–153. doi:10.1016/0305-1978(79)90024-3 DOI

Jacob, J., and Ziswiler. 1982. The uropygial gland. In: Farner, D. S., King J. R., and Parkes K. C., editors. Avian biology. New York: Academic Press; p. 199–322.

Jacob, S., Immer A., Leclaire S., Parthuisot N., Ducamp C., Espinasse G., and Heeb P.. . 2014. Uropygial gland size and composition varies according to experimentally modified microbiome in Great tits. BMC Evol. Biol. 14:134. doi:10.1186/1471-2148-14-134 PubMed DOI PMC

Jawad, H. S. A., Idris L. H., Bakar Z. B., and Kassim A. B.. . 2016a. Partial ablation of uropygial gland effect on carcass characteristics of Akar Putra chicken. Poult. Sci. 95:1966–1971. doi:10.3382/ps/pew125 PubMed DOI

Jawad, H. S., Lokman I. H., Zuki A. B., and Kassim A. B.. . 2016b. Partial ablation of uropygial gland effects on growth hormone concentration and digestive system histometrical aspect of Akar Putra chicken. Poult. Sci. 95:966–973. doi:10.3382/ps/pev444 PubMed DOI

Johnsson, M., Jonsson K. B., Andersson L., Jensen P., and Wright D.. . 2015. Quantitative trait locus and genetical genomics analysis identifies putatively causal genes for fecundity and brooding in the chicken. g3 (Bethesda). 6:311–319. doi:10.1534/g3.115.024299 PubMed DOI PMC

Kanakri, K., Muhlhausler B., Carragher J., Gibson R., Barekatain R., Dekoning C., Drake K., and Hughes R.. . 2018. Relationship between the fatty acid composition of uropygial gland secretion and blood of meat chickens receiving different dietary fats. Anim. Prod. Sci 58:828–833. doi:10.1071/an16268 DOI

Karlsson, A. C., Jensen P., Elgland M., Laur K., Fyrner T., Konradsson P., and Laska M.. . 2010. Red junglefowl have individual body odors. J. Exp. Biol. 213:1619–1624. doi:10.1242/jeb.040279 PubMed DOI

Kassambara, A. 2020. ggpubr: ‘ggplot2’ based publication ready plots. R package version 0.4.0.https://CRAN.R-project.org/package=ggpubr.

Kilpinen, O., Roepstorff A., Permin A., Nørgaard-Nielsen G., Lawson L. G., and Simonsen H. B.. . 2005. Influence of Dermanyssus gallinae and Ascaridia galli infections on behaviour and health of laying hens (Gallus gallus domesticus). Br. Poult. Sci. 46:26–34. doi:10.1080/00071660400023839 PubMed DOI

Kolattukudy, P. 2015. Wax Esters: chemistry and biosynthesis. In Pappas, A., editor. Lipids and skin health. Cham (UK): Springer; p. 159–183.

Kolattukudy, P. E., Bohnet S., and Rogers L.. . 1987. Diesters of 3-hydroxy fatty-acids produced by the uropygial glands of female mallards uniquely during the mating season. J. Lipid Res. 28:582–588. PubMed

Kolattukudy, P. E., and Sawaya W. N.. . 1974. Age dependent structural changes in the diol esters of uropygial glands of chicken. Lipids 9:290–292. doi:10.1007/BF02532208 PubMed DOI

Kuznetsova, A., Brockhoff P. B., and Christensen R. H. B.. . 2017. lmerTest package: tests in linear mixed effects models. J. Stat. Softw 82:1–26. doi:10.18637/jss.v082.i13 DOI

Lagerstrom, M. C., Hellstrom A. R., Gloriam D. E., Larsson T. P., Schioth H. B., and Fredriksson R.. . 2006. The G protein-coupled receptor subset of the chicken genome. PLoS Comput. Biol. 2:e54493–e54507. doi:10.1371/journal.pcbi.0020054 PubMed DOI PMC

Lambertz, C., Wuthijaree K., and Gauly M.. . 2018. Performance, behavior, and health of male broilers and laying hens of 2 dual-purpose chicken genotypes. Poult. Sci. 97:3564–3576. doi:10.3382/ps/pey223 PubMed DOI PMC

Leclaire, S., Merkling T., Raynaud C., Giacinti G., Bessière J. M., Hatch S. A., and Danchin E.. . 2011. An individual and a sex odor signature in kittiwakes?: study of the semiochemical composition of preen secretion and preen down feathers. Naturwissenschaften 98:615–624. doi:10.1007/s00114-011-0809-9 PubMed DOI

Leclaire, S., Pierret P., Chatelain M., and Gasparini J.. . 2014a. Feather bacterial load affects plumage condition, iridescent color, and investment in preening in pigeons. Behav. Ecol. 25:1192–1198. doi:10.1093/beheco/aru109 DOI

Leclaire, S., van Dongen W. F., Voccia S., Merkling T., Ducamp C., Hatch S. A., Blanchard P., Danchin E., and Wagner R. H.. . 2014b. Preen secretions encode information on MHC similarity in certain sex-dyads in a monogamous seabird. Sci. Rep. 4:6920. doi:10.1038/srep06920 PubMed DOI PMC

Lenth, R. V. 2016. Least-squares means: the R package lsmeans. J. Stat. Softw 69:1–33. doi:10.18637/jss.v069.i01 DOI

Lillard, D. A., and Toledo R. T.. . 1976. Isolation and characterization of lipids from chicken preen gland. J. Food Sci. 41:195–196. doi:10.1111/j.1365-2621.1976.tb01134.x DOI

López-Perea, J. J., and Mateo R.. . 2019. Wax esters of uropygial gland secretion as biomarkers of endocrine disruption in birds exposed to treated sewage water. Environ. Pollut. 250:323–330. doi:10.1016/j.envpol.2019.04.039 PubMed DOI

Lüdecke, D., Ben-Shachar M., Patil I., Waggoner P., and Makowski D.. . 2021. performance: an R package for assessment, comparison and testing of statistical models. J. Open Source Softw 6:3139. doi:10.21105/joss.03139 DOI

Madec, I., Gabarrou J. F., Saffray D., and Pageat P.. . 2008. Broilers (Gallus gallus) are less stressed if they can smell a mother odorant. South Afr. J. Anim. Sci. 38:201–206. https://hdl.handle.net/10520/EJC94579

Magallanes, S., Moller A. P., Garcia-Longoria L., de Lope F., and Marzal A.. . 2016. Volume and antimicrobial activity of secretions of the uropygial gland are correlated with malaria infection in house sparrows. Parasit. Vectors 9:8. doi:10.1186/s13071-016-1512-7 PubMed DOI PMC

Martin-Vivaldi, M., Ruiz-Rodriguez M., Soler J. J., Peralta-Sanchez J. M., Mendez M., Valdivia E., Martin-Platero A. M., and Martinez-Bueno M.. . 2009. Seasonal, sexual and developmental differences in hoopoe Upupa epops preen gland morphology and secretions: evidence for a role of bacteria. J. Avian Biol. 40:191–205. doi:10.1111/j.1600-048X.2009.04393.x DOI

Martín-Vivaldi, M., Soler J. J., Peralta-Sánchez J. M., Arco L., Martín-Platero A. M., Martínez-Bueno M., Ruiz-Rodríguez M., and Valdivia E.. . 2014. Special structures of hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching success. J. Anim. Ecol. 83:1289–1301. doi:10.1111/1365-2656.12243 PubMed DOI

Moller, A. P., Czirjak G. A., and Heeb P.. . 2009. Feather micro-organisms and uropygial antimicrobial defences in a colonial ­passerine bird. Funct. Ecol. 23:1097–1102. doi:10.1111/j.1365-2435.2009.01594.x DOI

Moller, A. P., and Mateos-Gonzalez F.. . 2019. Plumage brightness and uropygial gland secretions in Barn Swallows. Curr. Zool. 65:177–182. doi:10.1093/cz/zoy042 PubMed DOI PMC

Moreno-Rueda, G. 2010. Uropygial gland size correlates with feather holes, body condition and wingbar size in the House Sparrow Passer domesticus. J. Avian Biol. 41:229–236. doi:10.1111/j.1600-048x.2009.04859.x DOI

Moreno-Rueda, G. 2015. Body-mass-dependent trade-off between immune response and uropygial gland size in House Sparrows Passer domesticus. J. Avian Biol. 46:40–45. doi:10.1111/jav.00358 DOI

Moreno-Rueda, G. 2016. Uropygial gland and bib colouration in the house sparrow. PeerJ 4:e2102. doi:10.7717/peerj.2102 PubMed DOI PMC

Moreno-Rueda, G. 2017. Preen oil and bird fitness: a critical review of the evidence. Biol. Rev. Camb. Philos. Soc. 92:2131–2143. doi:10.1111/brv.12324 PubMed DOI

Mundry, R., and Nunn C. L.. . 2009. Stepwise model fitting and statistical inference: turning noise into signal pollution. Am. Nat. 173:119–123. doi:10.1086/593303 PubMed DOI

Naji, S. A. H., Al-Shammeri J. S., Jawad H. S. A., Lokman I. H., Zukia A. B. Z., and Kassimb A. B.. . 2020. The effect of uropygialectomy on productive performance of Japanese quails. Biochem. Cell. Arch. 20:2711–2714. doi:10.35124/bca.2020.20.1.2711 DOI

Pageat, P. 2010. Avian appeasing pheromones to decrease stress, anxiety and aggressiveness. Off. Gaz. U. S. Pat. Trademark Off. Pat.

Pan, P. R., Dilworth B. C., Day E. J., and Chen T. C.. . 1979. Effect of season of the year, sex, and dietary fats on broiler performance, abdominal fat, and preen gland secretion. Poult. Sci. 58:1564–1574. doi:10.3382/ps.0581564 DOI

Pap, P. L., Vagasi C. I., Barbos L., and Marton A.. . 2013. Chronic coccidian infestation compromises flight feather quality in House Sparrows Passer domesticus. Biol. J. Linn. Soc. 108:414–428. doi:10.1111/j.1095-8312.2012.02029.x DOI

Pap, P. L., Vagasi C. I., Osvath G., Muresan C., and Barta Z.. . 2010. Seasonality in the uropygial gland size and feather mite abundance in House Sparrows Passer domesticus: natural covariation and an experiment. J. Avian Biol. 41:653–661. doi:10.1111/j.1600-048X.2010.05146.x DOI

Piault, R., Gasparini J., Bize P., Paulet M., McGraw K. J., and Roulin A.. . 2008. Experimental support for the makeup hypothesis in nestling Tawny Owls (Strix aluco). Behav. Ecol.19:703–709. doi:10.1093/beheco/arm152 DOI

Potier, S., Besnard M. M., Schikorski D., Buatois B., Duriez O., Gabirot M., Leclaire S., and Bonadonna F.. . 2018. Preen oil chemical composition encodes individuality, seasonal variation and kinship in Black Kites Milvus migrans. J. Avian Biol. 49:e01728. doi:10.1111/jav.01728 DOI

Ruiz-Rodriguez, M., Tomas G., Martin-Galvez D., Ruiz-Castellano C., and Soler J. J.. . 2015. Bacteria and the evolution of honest signals. The case of ornamental throat feathers in spotless starlings. Funct. Ecol. 29:701–709. doi:10.1111/1365-2435.12376 DOI

Ruiz-Rodríguez, M., Valdivia E., Soler J. J., Martín-Vivaldi M., Martín-Platero A. M., and Martínez-Bueno M.. . 2009. Symbiotic bacteria living in the hoopoe’s uropygial gland prevent feather degradation. J. Exp. Biol. 212:3621–3626. doi:10.1242/jeb.031336 PubMed DOI

Saito, K., and Gamo M.. . 1968. The distribution of unusual fatty acids in preen gland lipids. J. Biochem. 64:557–559. doi:10.1093/oxfordjournals.jbchem.a128929 PubMed DOI

Sandilands, V., Savory J., and Powell K.. . 2004. Preen gland function in layer fowls: factors affecting morphology and feather lipid levels. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 137:217–225. doi:10.1016/j.cbpb.2003.10.004 PubMed DOI

Shawkey, M. D., Pillai S. R., and Hill G. E.. . 2003. Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J. Avian Biol. 34:345–349. doi:10.1111/j.0908-8857.2003.03193.x DOI

Soini, H. A., Schrock S. E., Bruce K. E., Wiesler D., Ketterson E. D., and Novotny M. V.. . 2007. Seasonal variation in volatile compound ­profiles of preen gland secretions of the dark-eyed junco (Junco hyemalis). J. Chem. Ecol. 33:183–198. doi:10.1007/s10886-006-9210-0 PubMed DOI

Soini, H. A., Whittaker D. J., Wiesler D., Ketterson E. D., and Novotny M. V.. . 2013. Chemosignaling diversity in songbirds: chromatographic profiling of preen oil volatiles in different species. J. Chromatogr. A 1317:186–192. doi:10.1016/j.chroma.2013.08.006 PubMed DOI

Steiger, S. S., Fidler A. E., Valcu M., and Kempenaers B.. . 2008. Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds? Proc. Biol. Sci. 275:2309–2317. doi:10.1098/rspb.2008.0607 PubMed DOI PMC

Stein, S. E. 1999. An integrated method for spectrum extraction and compound identification from gas chromatography/mass spectrometry data. J. Am. Soc. Mass. Spectrom. 10:770–781. doi:10.1016/S1044-0305(99)00047-1 DOI

Stettenheim, P. R. 2000. The integumentary morphology of modern birds - An overview. Am. Zool. 40:461–477. doi:10.1093/icb/40.4.461 DOI

Sweeney, R. J., Lovette I. J., and Harvey E. L.. . 2004. Evolutionary variation in feather waxes of passerine birds. Auk 121:435–445. doi:10.1642/0004-8038(2004)121[0435:evifwo]2.0.co;2 DOI

Tarsani, E., Kranis A., Maniatis G., Hager-Theodorides A. L., and Kominakis A.. . 2021. Detection of loci exhibiting pleiotropic effects on body weight and egg number in female broilers. Sci. Rep. 11:7441. doi:10.1038/s41598-021-86817-8 PubMed DOI PMC

RStudio Team. 2015. RStudio: integrated development for R. Boston (MA): RStudio, Inc.http://www.rstudio.com/

R Core Team. 2020. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing. http://www.r-project.org/index.html

Tona, K., Onagbesan O. M., Kamers B., Everaert N., Bruggeman V., and Decuypere E.. . 2010. Comparison of Cobb and Ross strains in embryo physiology and chick juvenile growth. Poult. Sci. 89:1677–1683. doi:10.3382/ps.2009-00386 PubMed DOI

Tůmová, E., Chodová D., Skřivanová E., Laloučková K., Šubrtová-Salmonová H., Ketta M., Machander V., and Cotozzolo E.. . 2021. Research note: the effects of genotype, sex, and feeding regime on performance, carcasses characteristic, and microbiota in chickens. Poult. Sci. 100:760–764. doi:10.1016/j.psj.2020.11.047 PubMed DOI PMC

Vanliere, D. W., Aggrey S. E., Brouns F. M. R., and Wiepkema P. R.. . 1991. Oiling behavior and the effect of lipids on dustbathing behavior in laying hens Gallus gallus domesticus. Behav. Proc. 24:71–81. doi:10.1016/0376-6357(91)90088-h PubMed DOI

Verea, C., Vitelli-Flores J., Isturiz T., Rodriguez-Lemoine V., and Bosque C.. . 2017. The effect of uropygial gland secretions of Spectacled Thrushes (Turdus nudigenis) on feather degradation and bacterial growth in vitro. J. Ornithol. 158:1035–1043. doi:10.1007/s10336-017-1461-8 DOI

Vincze, O., Vagasi C. I., Kovacs I., Galvan I., and Pap P. L.. . 2013. Sources of variation in uropygial gland size in European birds. Biol. J. Linn. Soc. 110:543–563. doi:10.1111/bij.12139 DOI

Wertz, P. W., Stover P. M., and Downing D. T.. . 1986. A survey of polar and nonpolar lipids from epidermis and epidermal appendages of the chicken (Gallus domesticus). Comp. Biochem. Physiol. B 84:203–206. doi:10.1016/0305-0491(86)90206-3 PubMed DOI

Wickham, H. 2016. ggplot2: elegant graphics for data analysis. New York (NY): Springer-Verlag. doi:10.1007/978-3-319-24277-4 DOI

Whittaker, D. J., Gerlach N. M., Soini H. A., Novotny M. V., and Ketterson E. D.. . 2013. Bird odour predicts reproductive success. Anim. Behav. 86:697–703. doi:10.1016/j.anbehav.2013.07.025 DOI

Whittaker, D. J., Richmond K. M., Miller A. K., Kiley R., Burns C. B., Atwell J. W., and Ketterson E. D.. . 2011. Intraspecific preen oil odor preferences in Dark-eyed Juncos (Junco hyemalis). Behav. Ecol. 22:1256–1263. doi:10.1093/beheco/arr122 DOI

Whittaker, D. J., Soini H. A., Atwell J. W., Hollars C., Novotny M. V., and Ketterson E. D.. . 2010. Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations. Behav. Ecol. 21:608–614. doi:10.1093/beheco/arq033 PubMed DOI PMC

Williams, C. R., Kokkinn M. J., and Smith B. P.. . 2003. Intraspecific variation in odor-mediated host preference of the mosquito Culex annulirostris. J. Chem. Ecol. 29:1889–1903. doi:10.1023/a:1024806429366 PubMed DOI

Wright, D., Rubin C. J., Martinez Barrio A., Schütz K., Kerje S., Brändström H., Kindmark A., Jensen P., and Andersson L.. . 2010. The genetic architecture of domestication in the chicken: effects of pleiotropy and linkage. Mol. Ecol. 19:5140–5156. doi:10.1111/j.1365-294X.2010.04882.x PubMed DOI

Wurdinger, I. 1982. Olfaction and home learning in juvenile geese (Anser-species and Branta-species). Biol. Behav. 7:347–351. doi:10.1111/j.1439-0310.1979.tb00281.x DOI

Zhang, J. -X., Sun L., and Zuo M. -X.. . 2009. Uropygial gland volatiles may code for olfactory information about sex, individual, and species in Bengalese finches Lonchura striata. Curr. Zool. 55:357–365. doi:10.1093/czoolo/55.5.357 DOI

Zhang, J. X., Wei W., Zhang J. H., and Yang W. H.. . 2010. Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars. Chem. Senses 35:375–382. doi:10.1093/chemse/bjq025 PubMed DOI